Vol. 445: 209–218, 2012 MARINE ECOLOGY PROGRESS SERIES Published January 20 doi: 10.3354/meps09460 Mar Ecol Prog Ser

Trans-Atlantic rafting by the brooding reef coral fragum on man-made flotsam

Bert W. Hoeksema1,* Piet J. Roos2,4 Gerhard C. Cadée3

Department of Marine Zoology, Netherlands Centre for Biodiversity Naturalis, PO Box 9517, 2300 RA Leiden, The Netherlands 2Netherlands Centre for Biodiversity Naturalis (Section ZMA), University of Amsterdam, PO Box 94766, 1090 GT Amsterdam, The Netherlands 3Royal Netherlands Institute for Sea Research, PO Box 59, 1790 AB Den Burg, Texel, The Netherlands

4Present address: Rembrandt van Rijnweg 8, 1191 GG Ouderkerk aan de Amstel, The Netherlands

ABSTRACT: Specimens of the brooding reef coral were found on man-made flotsam stranded on the North Sea shore of the Netherlands. Based on the associated epifauna originating from the southeast USA, we estimate that the corals must have crossed the Atlantic Ocean, trans- ported by the Gulf Stream and the North Atlantic Drift. The size of the corals suggests that they might have had enough time to cross the Atlantic alive and that they already reached the age of possible self-fertilization before they entered waters that were too cold to survive. The tempera- ture requirements and the presently known geographic range of F. fragum are compared with Atlantic summer and winter isotherms and oceanic currents in order to project a hypothetical northernmost range boundary. With increasing pollution, man-made flotsam may become a progressively more common substrate for reef corals that depend on rafting for long-distance dispersal. Eventually, with warming seawater, floating debris may cause tropical marine to expand their distribution ranges towards higher latitudes.

KEY WORDS: Distribution range · Epifauna · Life history · Long-distance dispersal · Ocean currents · Temperature tolerance

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INTRODUCTION dent on beaches around the world (Harrold & Lisin 1989, Thiel & Gutow 2005a). Many species of shallow-water marine benthic Anthropogenic flotsam and jetsam consisting of invertebrates use rafting for long-distance dispersal. non-biodegradable debris have a long durability and Buoyant plant material, such as macroalgae thalli, increasingly are becoming more common on beaches seagrass leaves, and driftwood, is commonly known than natural floating substrata (Thiel & Gutow as a biotic carrier for epifaunal communities despite 2005a). The litter usually originates from land via exposure to air, strong temperature fluctuations, and river mouths and drainage outlets and rarely as a harmful UV-radiation at the sea surface (Cheng result of storms and tsunamis. Shipping activities 1975, Thiel & Gutow 2005a,b, Fraser et al. 2011). The (merchant vessels), offshore industry, fisheries, and success of dispersal depends on the size, buoyancy, garbage dumping by coastal communities may also and permanence of the floating substrate (particu- play a role in the production of marine debris, larly if organic), the longevity of the sessile phase in although only part of it is floating (Jones 1995, Hess their life cycle, and the course and velocity of the car- et al. 1999, Donohue et al. 2001, Thiel & Gutow rying currents and winds. Eventually the floating 2005a, Richards & Beger 2011), and predominantly objects may become cast up onshore, which is evi- consists of fisheries gear and packaging materials

*Email: [email protected] © Inter-Research 2012 · www.int-res.com 210 Mar Ecol Prog Ser 445: 209–218, 2012

Fig. 1. Favia fragum. Gas cylinder (1.5 m long) with remnants of tropical epifauna washed ashore on the North Sea beach of Texel, The Netherlands. (a) The cylinder probably 3 yr after its stranding (positions of corals encircled). (b) Dead encrusting coral on cylinder together with an empty tube of a serpulid polychaete and a shell of the bivalve Chama congregata. (c) Specimens removed from their rusty substrate (RMNH Coel. 39909; scale bar: 1 cm)

(Uneputty & Evans 1997, Willoughby et al. 1997, vived for a long time. So far, it has only been hypoth- Derraik 2002, Thiel et al. 2003, Taffs & Cullen 2005, esised that the wide distribution range of brooding Gregory 2009, Ryan et al. 2009). organisms, and F. fragum in particular, may be The growth in man-made flotsam also causes an caused by long-distance dispersal through rafting increase of buoyant substrate for benthic organisms, (Highsmith 1985, Goodbody-Gringley et al. 2010). which has become most evident in areas where it Based on the species composition of the epifauna of used to be rare (Barnes 2002, Aliani & Molcard 2003). the cylinder, the course of oceanic currents, the size Fouling organisms are able to reach remote coast- and growth form of the corals, and information on the lines as long as their growing weight does not nega- biogeography and life history of F. fragum, we recon- tively affect the buoyancy of their substrate. Eventu- struct a scenario in order to explain how these reef ally, long-lasting flotsam can become responsible for corals were able to reach the temperate coastline of the introduction of exotic species (Winston 1982, the Netherlands. Winston et al. 1997, Barnes & Fraser 2003, Barnes & Milner 2005). When these exotic species appear to colonize new areas and become harmful to allochto- MATERIALS AND METHODS nous species, it is important to know their origin and natural environment for their control. A 1.5 m long, rusty metal gas cylinder covered by Recently, several specimens of the brooding amphi- abraded encrusting tropical epifaunal remains (Fig. 1a) Atlantic reef coral Favia fragum (Esper, 1793), to - was examined (29 November 2009) on the North gether with other fouling , were discovered on Sea beach of Texel, the westernmost of the Frisian a gas cylinder that was beached on Texel, the Nether- Islands. A report in the local newspaper resulted in lands, (Fig. 1). Although the corals were dead, they comments from readers testifying that the cylinder were large enough to tell that they must have sur- must have been lying there for at least 3 yr. The epi- Hoeksema et al.: Trans-Atlantic rafting by Favia fragum 211

fauna consisted of several specimens of the Atlantic pared the distribution range of Favia fragum with the coral Favia fragum, barnacles, bryozoans, serpulids, course of North Atlantic currents in order to retrace and bivalves. The encrusting corals were removed the cylinder’s journey. Furthermore we reviewed the from the metal cylinder with a knife to enable their life history and habitat requirements of the species identification using a binocular dissecting micro- and compared these with summer and winter surface scope. They were compared with an illustration of seawater isotherms in order to estimate the age of the the type specimen of F. fragum (Esper, 1793) and corals and how far they could have travelled when with specimens from various localities in the coelen- still alive. terate reference collection of Netherlands Centre for Biodiversity Naturalis, Leiden Naturalis (catalogued as RMNH Coel. and ZMA Coel.) in order to verify RESULTS their identity. They were also compared with the types of F. gravida (Verrill, 1868), which also has Identity of the beached corals an amphi-Atlantic distribution range (Laborel 1974, Hoeksema 2012). These specimens (YPM 1465a, The beached corals were small (∅ < 5.5 cm) and 1465b, 4549) were sent on loan from the Yale Peabody encrusting (Fig. 1). Despite their abraded condition, Museum of Harvard University at New Haven, Con- they could be identified as Favia fragum based on necticut, USA. skeletal characters when compared to undamaged After the analysis, 2 beached specimens (Fig. 1c) specimens (Fig. 2). F. fragum shows much variation were deposited in the collection of NCB Naturalis as in skeleton morphology (Roos 1971). The corals are reference material (RMNH Coel. 39909). We com- usually small (∅ < 10 cm), encrusting or massive and

Fig. 2. Favia fragum. Morphological similarity of encrusting coral from the West and East Atlantic. Specimens from (a,b) Curaçao, formerly part of the Netherlands Antilles (Piscadera Bay, collected on 18 March 1974; ZMA Coel. 7568) and (c,d) the Cape Verde islands (SW coast of Sao Vicente, San Pedro Bay, collected on 21 June 1982; RMNH Coel. 16978). Scale bar: 1 cm (applies to all panels) 212 Mar Ecol Prog Ser 445: 209–218, 2012

Fig. 3. Favia fragum and F. gravid. (a) Distribution ranges (after Laborel 1974, Aronson et al. 2008). The location of the dead beached specimens is indicated by a red star. (b) Course of the Gulf Stream and North Atlantic Drift from the Caribbean to western Europe (red = warm water current, blue = cool water current; http://www.noc.soton.ac.uk/ rapid/ sis/ popups/ gulf_stream.php; used with permission from National Oceanography Centre, Southampton; see also USASF 1943) spherical, with small corallites (∅ < 0.5 cm), and an The distribution of Favia fragum ranges from the irregular septal ornamentation (Roos 1971, Fig. 2). Caribbean and Bermuda (northernmost locality) to The type of F. fragum from ‘the southern American the Cape Verde Islands (Laborel 1974, Boekschoten seas’ (translated from Esper 1795) is missing (Scheer & Borel Best 1988, Fig. 3a). The skeleton morphology 1990), but Esper’s (1793) illustrations are clear does not show clear intraspecific variation between enough to confirm the identity of our specimens. the west and east Atlantic (Fig. 2) and can therefore Hoeksema et al.: Trans-Atlantic rafting by Favia fragum 213

not help to indicate the origin of the beached speci- after which the cylinder became inhabited by the mens. bivalve Timoclea grus at the southeastern coastline The species resembles its congener Favia gravida, of the USA along the Gulf Stream track (Fig. 3b). a predominantly littoral species with longer calices. Various estimates have been made regarding the Both species have amphi-Atlantic distributions but expected time interval for passive eastward long- they are genetically distant species (Nunes et al. 2008, range dispersal from the southeastern USA to west- 2011) and show no range overlap (Laborel 1974, Hoek- ern Europe, ranging at least 14 to 18 mo (Guppy sema in press, Fig. 3a). 1917, Cadée 2008, Bonhommeau et al. 2009), but if the cylinder would have entered the Columbus gyre, the expected travel time could have lasted 3 yr Origin of the marine fauna on the stranded extra or more (Ebbesmeyer & Scigliano 2009). The gas cylinder corals themselves were not overgrown by other or- ganisms (like barnacles), which indicates that they The remains of the other epifauna helped to recon- may have been dead for a short time when the struct its west Atlantic origin (Cadée & Cadée- cylinder washed ashore. Coenen 2010). A small bivalve hidden in one of the barnacles belongs to the gray pygmy venus shell Timoclea grus (Holmes, 1858), which has a distribu- Settlement and age of rafting corals: a life history tion range from Louisiana and the west coast of Florida to the Atlantic coast of Florida and North Car- In order to be a successful rafter a species needs a olina, southeast USA (Tucker Abott 1954, Warmke & life-history strategy that facilitates settlement on Tucker Abott 1961, Turgeon et al. 2009). Representa- floating substrates, and it has to live long enough to tives of 2 other bivalves belong to species with a sub- reach a suitable destination. The brooding coral tropical amphi-Atlantic distribution: the crested oys- Favia fragum is a simultaneous hermaphrodite with ter Ostrea equestris (Say, 1834) and the corrugate high rates of self-fertilization during lunar cycles of jewelbox Chama congregata (Conrad, 1833). Shells gametogenesis and planulation (Szmant-Froelich et of bivalves with an even wider, more northward al. 1985, Brazeau et al. 1998, Gleason et al. 2001, Atlantic distribution range were also present, i.e. Carlon 2002, Goodbody-Gringley 2010). Planulation Hiatella arctica (Linnaeus, 1767) and Gastrochaena is monthly throughout the year in the Caribbean dubia (Pennant, 1777). The barnacles covering large (Szmant 1986, Soong 1991) or seasonal at higher parts of the cylinder belong to Balanus trigonus Dar- latitude (Bermuda), usually taking place before the win, 1854, originally a Pacific species but now dis- water temperature reaches its maximum (Goodbody- persed worldwide in the subtropical seas as fouling Gringley & de Putron 2009). Therefore the corals on on ships (Cadée 2011). The subtropical species rep- the cylinder must have settled when the cylinder was resented on the gas cylinder, in particular Favia in close proximity to a reef where planulation took fragum and T. grus, have overlapping distribution place, most likely year-round. ranges in southern Florida. Favia fragum larvae survive only a few days after release. They are initially phototaxic but become rapidly negatively buoyant and settle on dark sur- DISCUSSION faces in clusters close to their parents (Lewis 1974a,b, Carlon & Olson 1993, Carlon 2002, Petersen et al. The Gulfstream track 2007, Norström & Sandström 2010). They prefer hor- izontal, flat, uneven surfaces for settlement (Petersen Within the geographical range of Favia fragum, et al. 2005a,b, 2007). Because the cylinder was float- the Cape Verde Islands are the closest locality to ing (reaching not deeper than 1.5 m), the larvae the Netherlands (Fig. 3a). However, it is doubtful probably settled on it when they were still photo- that the Texel specimens came from there because taxic. The cylinder may already have been rusty at there are no oceanic currents that confirm such a that time (Fig. 1), providing the larvae with a rough track (Fig. 3b). Based on the course of the Gulf surface for attachment. In shallow water, the cylinder Stream and the North Atlantic Drift and the range may have been touching the reef bottom but during overlap of the associated fauna on the cylinder, the its journey in open water, it could have been deeply most likely origin would be southern Florida. The submerged and perhaps in vertical position consider- corals could also have settled in the Caribbean, ing its heavy weight. 214 Mar Ecol Prog Ser 445: 209–218, 2012

The corals on the cylinder were relatively large the shaded side of a floating substrate, recruits risk (5.5 cm). In their first 2 to 4 yr Favia fragum corals exposure to air and sunlight if the drifting substrate grow rapidly, after which they grow more slowly rolls over. Nevertheless, corals of this shallow-water (Vaughan 1916). They have been estimated to grow species are well able to resist heat exposure and 16 mm in diameter per year in a growth range from show much intraspecific morphological variation, 11 to 27 mm (Van Moorsel 1988). They have a fast which enables them to survive in various environ- generation turnover and can become fertile within ments (Roos 1971, Carlon & Budd 2002). 1 yr, implying that they reach maturity when they are Eventually, rafting corals die when they reach cold still very small with even marginal polyps able to water and they are not successful colonizers unless produce gonads (Soong & Lang 1992, Petersen et al. their offspring reach a suitable substrate first. 2007). The maximum corallum size in F. fragum is Edinger & Risk (1994) considered Favia fragum cold- smaller (<10 cm) in comparison with many other tolerant compared to other Caribbean corals. Adult Atlantic coral species and appears to be related to its F. fragum are also able to endure cold water (14°C) reproductive strategy as a brooder (Vaughan 1916, for short periods but not without damage (Mayer Soong 1993). They start to die when they reach a size 1914), which agrees with the general pattern that at which other species are considered juveniles Atlantic reef corals are sensitive to temperatures (Edmunds 2000). The corals on the cylinder may below 16°C (Burns 1985). This implies that the range have been about 3 yr old when they died, which limits for F. fragum depend on seasonal temperature would have given them more than enough time to fluctuations (Fig. 4). They may survive travel longer survive up to 14 to 18 mo and cross over the Atlantic. in the summer than in winter, but eventually they are If they had reached a suitable habitat, they may also limited by minimum winter temperatures. In their have been able to reproduce soon after due to early present range, Bermuda in the West Atlantic appears maturity and self-fertilization. to be the coldest area where they persevere, with a minimum temperature of 20°C (Figs. 3 & 4), whereas surface water in the more southward Cape Verde Rafting opportunities: substratum and depth Islands in the East Atlantic is about 22°C. preferences

In order to use rafting as a means for long-range Natural substrates of rafting corals dispersal, Favia fragum must be able to live on float- ing substrates. Favia fragum is able to grow on many Jackson (1986) argued that the wide distribution kinds of shallow water substrates (<15 m, predomi- ranges of brooding Atlantic reef corals (including nantly <3 m depth), including inland waters (Roos Favia fragum) can only be explained by rafting. Some 1971, Bak 1975, Carlon 2002). They generally grow reef corals are known to become floatable after expo- on solid substrate remote from sand, which may even sure to air without a floating substrate (Kornicker & consist of erect branches of alcyonarians (Kissling Squires 1962). Although, driftwood in the form of 1965). F. fragum has been found growing on man- trees is used by many rafting organisms (Thiel & Haye grove prop roots but with no mention of potential 2006), this has not yet been observed for corals. A buoyancy and dispersal (Roos 1964, 1971, Rogers likely natural substrate for rafting reef corals is vol- 2009). Their larvae can settle on thalli of the calcare- canic drift pumice (Jokiel 1984, 1989, 1990a,b, Jokiel ous green alga Halimeda opuntia, although it is not & Cox 2003), which has indeed been reported from expected that recruits will reach adult size due to the the North Atlantic (Binns 1972) and may stay afloat short life span of the thallus segments (Nugues & long enough to enable dispersal by rafting (Whitham Szmant 2006). Because the species occurs at both & Sparks 1986, Bravo et al. 2011). Dead unattached sides of the Atlantic, it may use firm floating sub- corals may become buoyant due to gas production and strates for long-distance dispersal, which is sup- become rafting substrates themselves (De Vantier 1992). ported by the present observation. Adult Favia fragum corals may resist exposure to air and high temperatures, enabling them to survive Rafting corals on man-made substrates in shallow water heated by the sun (Vaughan 1916, Mayer 1917). On the other hand, their larvae cannot There is little information on rafting by corals on endure long exposure to elevated seawater tempera- anthropogenic substrates. All available records con- ture (31°C) (Randall & Szmant 2009). If they settle on cern dead specimens. Boekschoten & Borel Best Hoeksema et al.: Trans-Atlantic rafting by Favia fragum 215

Fig. 4. (a) Winter (February) and (b) summer (August) isotherms of surface water in the northern Atlantic (source Cambridge et al. 1987)

(1988) argue that the presence of dead Favia corals Adema 1987, 1995) concern dead specimens of on Brazilian cobbles along Cape Verdian coastlines Northeast Atlantic species (Zibrowius 1980), like can be explained by their use as ballast in salt vessels azooxanthellate Devonshire cup corals, Caryophyllia from Brazil. They resemble F. gravida corals from the smithii Stokes & Broderip, 1828, on various plastic coast of West Africa and Brazilian waters (Laborel objects and a piece of bitumen, and specimens of 1974, Amaral & Ramos 2007). Thalamophyllia gasti (Döderlein, 1913) on a glass The present case of Favia fragum corals reaching fish net buoy. These records suggest that man-made the Netherlands is the first record of a tropical zoox- objects may serve well as substrates for corals, anthellate coral species for the North Sea. Previous which may enlarge their chances for long-distance records of scleractinians in the Netherlands (e.g. dispersal. 216 Mar Ecol Prog Ser 445: 209–218, 2012

Rafting corals and sea water warming Acknowledgements. V. Byfield (National Oceanography Centre, Southampton) gave permission for use of Fig. 3b. The type specimens of Favia gravida were sent on loan by E. Rising seawater temperatures will cause summer Lazo Wasem (Yale Peabody Museum, New Haven, CT) and and winter sea water surface isotherms to shift the specimens of F. fragum from Curaçao by E. Beglinger towards higher latitudes, which may facilitate the (Zoological Museum Amsterdam, ZMA). R.G. Moolenbeek settlement of zooxanthellate corals in areas where (ZMA) and J. Goud (Netherlands Centre for Biodiversity Naturalis, Leiden Naturalis) checked the identity of the they previously did not occur. Recent ex amples of mollusks. G.C.C. thanks the directors of the Royal NIOZ for range shifts among reef corals con cern species room and facilities they provide for him after his retirement. occurring along continuous coastlines (Florida, West Australia, Japan), possibly through larval dispersal (Precht & Aronson 2004, Greenstein & Pandolfi 2008, LITERATURE CITED Yamano et al. 2011). Examples of non-indigenous Adema JPHM (1987) Een glazen drijver van een visnet corals that showed range expansion after settlement aangespoeld op het strand tussen Katwijk en Noordwijk. are Indo-Pacific azooxanthellate Tubastraea species Het Zeepaard 47:146−152 entering the West Atlantic, most likely as fouling Adema JPHM (1995) De Nederlandse steenkoralen (Coe- lenterata, , ): een monografie. Het on ships or oil rigs (Fenner & Banks 2004, Hoek- Zeepaard 55: 96−100 sema et al. 2011, Mantelatto et al. 2011). 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Editorial responsibility: Charles Birkeland, Submitted: September 5, 2011; Accepted: October 22, 2011 Honolulu, Hawaii, USA Proofs received from author(s): January 3, 2012